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i Primates in Flooded Habitats Ecology and Conservation Nearly half the world’s primate species use flooded habitats at one time or another, from swamp- going Congo gorillas and mangrove-e ating proboscis monkeys, to uacaris in Amazonian riverside forests. This first- ever volume on the subject brings together experts from around the world in a ground- breaking volume spanning fossil history, current biology, and future research and conservation priorities. Flooded habitats are a vital part of tropical biology, both for the diversity of the species they house, and the complexity of their ecological interactions, but are often completely overlooked. This book will set the stage for a new wave of research on primates in these extraordinarily productive and highly threatened areas, and is ideal for researchers and graduate students in primatology, zoology, ecology, and conservation. Katarzyna Nowak is a Research Associate at the University of the Free State, Qwaqwa campus, South Africa and a Fellow at The Safina Center in New York. Her conservation research focuses on the behavioural flexibility of threatened species. Adrian A. Barnett is Lecturer and Researcher at the National Institute for Amazon Research, Brazil, and the Federal University of Amazonas, Brazil, and a Research Fellow at Roehampton University, UK. He has worked with flooded habitats and their primates for more than 25 years. Ikki Matsuda is an Associate Professor at the Chubu University Academy of Emerging Sciences and a member of both the Japan Monkey Centre (Advisor) and the Wildlife Research Center of Kyoto University (specially appointed Associate Professor) in Japan. He focuses on a synthetic understanding of the evolu- tion and ecology of colobine species, in particular of the proboscis monkey. ii iii Primates in Flooded Habitats Ecology and Conservation Edited by Katarzyna Nowak University of the Free State, South Africa Adrian A. Barnett National Institute for Amazon Research, Brazil Ikki Matsuda Chubu University/Kyoto University/Japan Monkey Centre, Japan iv University Printing House, Cambridge CB2 8BS, United Kingdom One Liberty Plaza, 20th Floor, New York, NY 10006, USA 477 Williamstown Road, Port Melbourne, VIC 3207, Australia 314– 321, 3rd Floor, Plot 3, Splendor Forum, Jasola District Centre, New Delhi – 110025, India 79 Anson Road, #06- 04/ 06, Singapore 079906 Cambridge University Press is part of the University of Cambridge. It furthers the University’s mission by disseminating knowledge in the pursuit of education, learning, and research at the highest international levels of excellence. www.cambridge.org Information on this title: www.cambridge.org/ 9781107134317 DOI: 10.1017/ 9781316466780 © Cambridge University Press 2019 This publication is in copyright. Subject to statutory exception and to the provisions of relevant collective licensing agreements, no reproduction of any part may take place without the written permission of Cambridge University Press. First published 2019 Printed in the United Kingdom by TJ International Ltd. Padstow Cornwall A catalogue record for this publication is available from the British Library. ISBN 978- 1- 107- 13431- 7 Hardback Additional resources for this publication at www.cambridge.org/9781107134317 Cambridge University Press has no responsibility for the persistence or accuracy of URLs for external or third- party internet websites referred to in this publication and does not guarantee that any content on such websites is, or will remain, accurate or appropriate. v Contents List of Contributors page ix Foreword xv Acknowledgements xvii Part I – Introduction 8 Mangrove- living Primates in the Neotropics: An Ecological Review 54 1 Editors’ Introduction 1 Ricardo Rodrigues dos Santos and LeAndra Luecke Katarzyna Nowak, Adrian A. Barnett and Bridgeman Ikki Matsuda 9 The Role of Tools in the Feeding Ecology of Bearded 2 Flooded and Riparian Habitats in the Capuchins Living in Mangroves 59 Tropics: Community Definitions and Ecological Ricardo Rodrigues dos Santos, Arrilton Araújo de Sousa, Summaries 2 Dorothy M. Fragaszy and Renata Gonçalves Ferreira Amy C. Bennett, Pia Parolin, Leandro V. Ferreira, 10 Use of Mangrove Habitats by Sapajus flavius Ikki Matsuda and Neil D. Burgess Assessed by Vocalization Surveys 64 3 Fossil Primates from Flooded Habitats: Monique Bastos, Karolina Medeiros, Antonio Souto, Gareth The Antiquity of an Association 10 Jones and Bruna M. Bezerra Matt Sponheimer, James E. Loudon and 11 Mangrove Forests as a Key Habitat for the Michaela E. Howells Conservation of the Critically Endangered Yellow- 4 Comparison of Plant Diversity and Phenology of breasted Capuchin, Sapajus xanthosternos, in the Riverine and Mangrove Forests with Those of the Brazilian Northeast 68 Dryland Forest in Sabah, Borneo, Malaysia 15 Raone Beltrão- Mendes and Stephen F. Ferrari Ikki Matsuda, Miyabi Nakabayashi, Yosuke Otani, 12 Primates of African Mangroves 77 Yap Sau Wai, Augustine Tuuga, Anna Wong, Josephine Head, Aoife Healy and Katarzyna Nowak Henry Bernard, Serge A. Wich and Takuya Kubo 13 Feeding Ecology of the Proboscis Monkey in Sabah, 5 Lemurs in Mangroves and Other Malaysia, with Special Reference to Plant Flooded Habitats 29 Species- Poor Forests 89 Giuseppe Donati, Timothy M. Eppley, José Ralison, Henry Bernard, Ikki Matsuda, Goro Hanya, Mui- How Jacky Youssouf and Jörg U. Ganzhorn Phua, Felicity Oram and Abdul Hamid Ahmad 6 Survey and Study Methods for Flooded Habitat 14 Ebony Langurs in Mangrove and Beach Forests of Primatology 33 Java, Bali and Lombok 99 Adrian A. Barnett, Joseph E. Hawes, Antonio R. Mendes Vincent Nijman Pontes, Viviane M. Guedes Layme, Janice Chism, Robert B. Wallace, Nayara de Alecântara Cardoso, 15 Mangrove: Possible Vector for Tarsier Dispersal Stephen F. Ferrari, Raone Beltrão- Mendes, Barth Wright, Across Open Ocean 105 Torbjørn Haugaasen, Rose Marie Hoare, Susan M. Cheyne, Myron Shekelle, Joan Stevenson, Blair Kaufer, Bruna M. Bezerra, Ikki Matsuda and Ricardo Rodrigues Steven Stilwell and Agus Salim dos Santos 16 Primates in the Sundarbans of India and Bangladesh 110 Part II – Primates of Mangrove and Jayanta Kumar Mallick Coastal Forests 17 Behavioural Ecology of Mangrove Primates and Their Neighbours 124 7 Worldwide Patterns in the Ecology of Ricardo Rodrigues dos Santos, LeAndra Luecke Bridgeman, Mangrove- living Monkeys and Apes 45 Jatna Supriatna, Rondang Siregar, Nurul Winarni and Katarzyna Nowak and Rebecca Coles Roberta Salmi v vi Contents Part III – Beach Primates 28 Primate Community Structure at Three Flooded Forest Sites in Guyana 226 18 Maritime Macaques: Ecological Background of Christopher A. Shaffer, Barth Wright and Kristin Wright Seafood Eating by Wild Japanese Macaques 29 Primates of the Peat Swamp in Borneo and (Macaca fuscata) 135 Sumatra 236 Yamato Tsuji and Nobuko Kazahari Susan M. Cheyne, Marcel Quinten and Keith Hodges 19 Long- tailed Macaque Stone Tool Use in Intertidal 30 Primates of Africa’s Coastal Deltas and Their Habitats 144 Conservation 244 Michael D. Gumert, Amanda Tan and Suchinda Thomas M. Butynski and Yvonne A. de Jong Malaivijitnond 31 Primates of Riverine and Gallery Forests: 20 The Ecology of Chacma Baboon Foraging in the A Worldwide Overview 259 Marine Intertidal Zone of the Cape Peninsula, Shawn Lehman, Kerriann McCoogan and Adrian South Africa 148 A. Barnett Matthew C. Lewis and M. Justin O’Riain 32 Life- history Traits and Group Dynamic in Black and Gold Howler Monkeys in Flooded Forests of Part IV – Swamp Primates Northern Argentina 263 Martin M. Kowalewski, Romina Pavé, Vanina A. 21 Primates and Flooded Forest in the Colombian Fernández, Mariana Raño and Gabriel E. Zunino Llanos 153 Xyomara Carretero- Pinzon and Thomas R. Defler 33 Riverine Red- tails: Preliminary Data on Forest Guenons in a Savanna Woodland Habitat in the Issa 22 Primates of the South American Pantanal Valley, Ugalla, Western Tanzania 270 Wetland: Seasonal Effects on Their Habitats and Simon Tapper, Caspian Johnson, Anna Lenoël, Alexander Habits 163 Vining, Fiona A. Stewart and Alex K. Piel Cleber J.R. Alho and Fernando C. Passos 34 Consequences of Lakeside Living for the Diet 23 Endangered Range- restricted Flooded Savanna and Social Ecology of the Lake Alaotran Gentle Titi Monkey Endemics Plecturocebus modestus and Lemur 276 P. olallae: Identifying Areas Vulnerable to Excess Patrick O. Waeber, Fidimalala B. Ralainasolo, Jonah Flooding, Fire and Deforestation in Southwestern H. Ratsimbazafy and Caroline M. Nievergelt Beni Department, Bolivia 172 Teddy Marcelo Siles Lazzo, Robert B. Wallace and 35 Non- leaping Slow Lorises: Ecological Constraints of Jesus Martinez Living in Flooded Habitats 279 Anna Nekaris, Denise Spaan and Vincent Nijman 24 Use of Swamp and Riverside Forest by Eastern and Western Gorillas 184 Juichi Yamagiwa, Yuji Iwata, Chieko Ando and Part VI – Conservation Case Studies A.K. Basabose 36 Dams: Implications of Widespread Anthropic 25 Use of Inundated Habitats by Great Apes in the Flooding for Primate Populations 285 Congo Basin: A Case Study of Swamp Forest Use Amy Harrison- Levine, Herbert H. Covert, Marilyn by Bonobos at Wamba, Democratic Republic of A. Norconk, Ricardo Rodrigues dos Santos, Adrian the Congo 195 A. Barnett and Philip Fearnside Saeko Terada, Janet Nackoney, Tetsuya Sakamaki, Mbangi Norbert Mulavwa, Takakazu Yumoto and 37 Hapalemur alaotrensis: A Conservation Case Study Takeshi Furuichi from the Swamps of Alaotra, Madagascar 293 Patrick O. Waeber, Jonah H. Ratsimbazafy, Herizo 26 Differences in Population Density of Orangutan Andrianandrasana, Fidimalala B. Ralainasolo and Between Flooded and Non- flooded Forests 212 Caroline M. Nievergelt Tomoko Kanamori, Noko Kuze and Shiro Kohshima 38 Landscape Genetics Applied to the Conservation of Primates in Flooded Forests: A Case Study of Part V – Primates in Freshwater Orangutans in the Lower Kinabatangan Wildlife Flooded Forests Sanctuary 297 Milena Salgado- Lynn, Mohammad Fairus B. Jalil, Lounès 27 Primates in Amazonian Flooded Habitats 217 Chikhi, Marc Ancrenaz, Laurentius N. Ambu, Michael Adrian A. Barnett W. Bruford and Benoît Goossens vi vii Contents 39 African Flooded Areas as Refuge Habitats 304 45 Conservation of Primates and Their Flooded Habitats Anh Galat- Luong, Gerard Galat, Rebecca Coles and in the Neotropics 359 Jan Nizinski Sarah A. Boyle, Cleber J.R. Alho, Janice Chism, Thomas R. Defler, Anthony Di Fiore, Eduardo Fernandez- Duque, 40 Diversity and Conservation of Primates in Erwin Palacios, Ricardo Rodrigues dos Santos, Christopher the Flooded Forests of Southern Nigeria 315 A. Shaffer, Claudia Regina da Silva, Bernardo Urbani, Lynne R. Baker and John F. Oates Robert Wallace, Barth Wright, Kristin Wright, Bruno de 41 Mamirauá Reserve: Primate- based Flooded Forest Freitas Xavier and Adrian A. Barnett Conservation in the Amazon 326 Nelissa Peralta, Hani R. El Bizri, Fernanda P. Paim and João Valsecchi 42 Primates in Flooded Forests of Borneo: References 375 Opportunities and Challenges for Ecotourism Index 443 as a Conservation Strategy 331 Stanislav Lhota, Katherine S.S. Scott and John Chih Colour plates can be found between pages 174 and 175. Mun Sha Part VII – Conservation, Threats and Status 43 Conservation Value of Africa’s Flooded Habitats to Non- human Primates 341 Katarzyna Nowak, Fiona Maisels, Lynne R. Baker and Hugo Rainey 44 Southeast Asian Primates in Flooded Forests 347 John Chih Mun Sha, Shun Deng Fam and Andie Hui Fang Ang vii viii